UC Santa Cruz UC Santa Cruz Previously Published Works Title Diversification of Trait Combinations in Coevolving Plant and Insect Lineages. Permalink https://escholarship.org/uc/item/86h2s0j3 Journal The American naturalist, 190(2) ISSN 0003-0147 Authors Thompson, John N Schwind, Christopher Friberg, Magne Publication Date 2017-08-01 DOI 10.1086/692164 Peer reviewed eScholarship.org Powered by the California Digital Library University of California vol. 190, no. 2 the american naturalist august 2017 Diversification of Trait Combinations in Coevolving Plant and Insect Lineages John N. Thompson,1,* Christopher Schwind,1 and Magne Friberg2 1. Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, California 95064; 2. Department of Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden Submitted October 17, 2016; Accepted March 15, 2017; Electronically published May 8, 2017 Online enhancements: appendix. abstract:Closely related species often have similar traits and some- 2002), and coevolution of wild parsnips and parsnip web- times interact with the same species. A crucial problem in evolution- worms differs when cow parsnips locally co-occur (Zangerl ary ecology is therefore to understand how coevolving species diverge and Berenbaum 2003). These and other studies have indi- when they interact with a set of closely related species from another cated that the coevolutionary process does not always favor lineage rather than with a single species. We evaluated geographic dif- pairs of coevolving species (Thompson 2005, 2013; Nuismer ferences in the floral morphology of all woodland star plant species et al. 2012; Poisot et al. 2012; Kagawa and Takimoto 2014). (Lithophragma, Saxifragaceae) that are pollinated by Greya (Prodoxi- Although coevolution between pairs of interacting species dae) moths. Flowers of each woodland star species differed depending on whether plants interact locally with one, two, or no pollinating moth can form geographic mosaics of traits and ecological out- species. Plants of one species grown in six different environments comes (Lorenzi and Thompson 2011; Gibert et al. 2013; showed few differences in floral traits, suggesting that the geographic Vergara et al. 2013; Hague et al. 2016), coevolution within differences are not due significantly to trait plasticity. Greya moth pop- networks of interacting species has the potential to form even ulations also showed significant geographic divergence in morphology, more complex geographic mosaics. Coevolution within lo- depending on the local host and on whether the moth species co- cal networks can act both directly and indirectly on each spe- occurred locally. Divergence in the plants and the moths involved shifts cies as each evolutionary change cascades throughout the net- in combinations of partially correlated traits, rather than any one trait. The results indicate that the geographic mosaic of coevolution can be work. Mathematical models of coevolution have shown that amplified as coevolving lineages diversify into separate species and the evolution of traits may differ when selection occurs within come together in different combinations in different ecosystems. networks rather than between pairs of species (Guimarães et al. 2011; Nuismer et al. 2012; Bascompte and Jordano fl Keywords: coevolution, complex traits, oral evolution, geographic 2013). mosaic. Networks can form as coevolving lineages diversify. Spe- cies that originally coevolved with only one species in an- Introduction other lineage may expand their interactions in some regions to include other congeners within that lineage. What began Coevolution between pairs of species is almost always em- as a globally pairwise interaction becomes a geographic mo- bedded in a geographically varying network of interactions saic of interacting species. Ongoing local loss or addition of with other species. For example, coevolution between lodge- species to an interaction, through range changes or other pole pines and crossbills differs when red squirrels co-occur ecological processes, may continually alter this mosaic, as in the same community (Benkman et al. 2010), coevolution has been documented in multiple studies (Brodie et al. 2002; of woodland star (Lithophragma) plants and Greya moths is Parchman and Benkman 2002; Zangerl and Berenbaum 2003; altered in a few localities by the presence of abundant soli- Lankau 2012; Stouffer et al. 2014; Newman et al. 2015; Pérez- fl tary bees or bombyliid ies (Thompson and Cunningham Méndez et al. 2016). How interactions assemble and evolve into local, regional, and global networks of different sizes * Corresponding author; e-mail: [email protected]. and phylogenetic configurations has therefore become a ma- ORCIDs: Thompson, http://orcid.org/0000-0001-5941-6498. jor problem to understand in coevolutionary biology (Jor- Am. Nat. 2017. Vol. 190, pp. 171–184. q 2017 by The University of Chicago. dano et al. 2003; Strauss et al. 2005; Thompson 2005, 2013; 0003-0147/2017/19002-57334$15.00. All rights reserved. This work is licensed Olesen et al. 2007; Hoeksema 2010; Jordano 2010; Nuismer under a Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits reuse of the work with attribution. et al. 2012; Bascompte and Jordano 2013; Wise and Rausher DOI: 10.1086/692164 2013; Heath and Stinchcombe 2014; Bronstein 2015; Parch- This content downloaded from 128.114.028.238 on July 30, 2018 12:35:47 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 172 The American Naturalist man et al. 2016). Addressing the problem requires large-scale ogy found within each species results in part from differ- analyses of how lineages of closely related species assemble ences among ecosystems in the combination of locally in- and coevolve with other lineages in different environmental teracting plant and moth species. This prediction follows contexts. from several past observations and results. First, popula- In some coevolving interactions, the focus of reciprocal tions of each woodland star species differ in whether they selection is sometimes on a particular trait in one species interact with one coevolving Greya moth species, two lo- that is countered or matched by a particular trait in another cally pollinating Greya species that differ in how they pol- species. Among the best-studied examples are the geographic linate flowers, or, more rarely, no locally coevolving Greya differences in the levels of tetrodotoxin in Taricha newts and moths. These interactions therefore have the potential to tolerance or detoxification of tetrodotoxin in Thamnophis produce not only a geographic mosaic of coevolution be- garter snakes (Brodie et al. 2002; Hague et al. 2016) or the size tween any one pair of interacting woodland star and Greya of Camellia fruits and the length of camellia weevils used to moth species but also a geographic and phylogenetic mosaic pierce the fruits to reach the seeds (Toju et al. 2011). In some of coevolving traits in plants and the moths. other coevolving interactions, however, the focus of selec- Second, Greya moth species differ in how they pollinate tion may be on a set of traits that are partially correlated but and lay their eggs in the reproductive parts of Lithophragma evolve to similar outcomes when exposed to similar selection plants (fig. 1). Greya politella females pollinate flowers mostly pressures. The now-classic example is the coevolution of the while ovipositing through the corolla, as pollen adhering to complex morphological traits of conifer cones and crossbill the abdomen rubs off onto the stigma. In most populations bills in different environments, in which the cones evolve to- of this species, females oviposit by piercing the base of the ward more conical or cylindrical forms depending on whether nectary disk with the ovipositor. While doing so, pollen ad- selection is driven by squirrels or crossbills (Benkman and hering to the membrane of the extended ovipositor rubs onto Mezquida 2015). In yet other interactions, selection could the stigma. In contrast, G. obscura moths pollinate flowers act on suites of partially correlated traits in ways that create only while nectaring. They then move to the base of the flower multiple evolutionary solutions even within a single lineage. to oviposit into the outer ovary wall or the scape (Thompson Previous work has suggested that the interactions between et al. 2010). Experimental studies have shown that although woodland stars (Lithophragma: Saxifragaceae) and Greya G. politella is a much more effective pollinator than G. ob- (Prodoxidae) moths have coevolved in this way (Thompson scura, G. obscura is often more abundant (Thompson et al. et al. 2013). Species and populations differ so widely in trait 2010, 2013). The relative effects of these moth species on combinations involved in the interaction that no single co- plant fitness could therefore vary among ecosystems. evolutionary solution is evident. Third, past studies have shown that fitness in the plants We therefore undertook an analysis of how multiple co- and the moths depends on their interaction in most locali- evolutionary solutions are clustered within and among all ties. Not only are Greya species associated with Lithophragma species of interacting woodland stars and Greya moths. specialized to feed as adults and larvae only on this plant ge- We predicted that the diversity of floral and